The contribution of commonly consumed edible insects to nutrition security in the Eastern D.R. Congo

Edible insects are perceived as an incredible opportunity to mitigate the major challenge of sustainably producing healthy foods for a growing world population in the face of climate change uncertainties over the coming decade. In this study, we assessed the nutrient composition and sensory properties of Acheta domesticus, Apis mellifera, Gnathocera trivittata, Gryllotalpa africana, Imbrasia epimethea, Imbrasia oyemensis, Locusta migratoria, Macrotermes subhylanus, Nomadacris septemfasciata, Rhyncophorus phoenicis, Ruspolia differens and Rhynchophorus ferrugineus consumed in Eastern D. R. Congo. The investigated edible insects are highly appreciated and nutritious, with proteins (20.67–43.93 g/100 g) and fats (14.53–36.02 g/100 g) being the major macro-nutrients, proving their potential to improve diets through food enrichment. The high potassium (24–386.67 mg/100 g), sodium (152–257.82 mg/100 g), magnesium (32–64 mg/100 g), iron (5.3–16.13 mg/100 g), calcium (25–156.67 mg/100 g) and zinc (11–19.67 mg/100 g) content make the assessed edible insects a useful mineral-containing ingredient for preventing undernutrition in countries which are plagued by micronutrient deficiencies. A scatter plot of matrices and Pearson’s correlations between sensory attributes and nutritional composition showed a negative correlation (r = − 0.45) between protein and appearance. While no strong correlation was observed between nutritional attributes and sensory acceptance, a positive correlation was observed between potassium and aroma (r = 0.50), after-taste (r = 0.50) and acceptability (r = 0.52). Principal component analysis results indicated that the two axes accounted for up to 97.4% of the observed variability in the nutrient composition and sensory attributes of commonly consumed edible insects in the Eastern D. R. Congo. Given the significant delicacy and nutritional potential of edible insects highlighted in this paper, households can rely on the latter to meet their nutritional needs rather than conventional livestock, thus contributing to environmental and financial security through local business opportunities.

the serious challenge of feeding people in the coming decades [5][6][7] .Given their nutritional potential 8 , taste 9,10 , economic benefits 11,12 , less land-dependent production 13 , high feed conversion efficiency compared to conventional livestock and relatively low emission of greenhouse gases 14 , and ammonia 15 , with sufficient biomass in some wild-harvested for commercial supply 16 , intensive rearing at both household level 17 , and industrial scale is recommended 18 .
The Republic Democratic of Congo (DRC) is known for its wide biodiversity including edible insects [24][25][26][27] , especially as the collection and trade of the latter and other non-timber forest products are legal activities encouraged by the 2002 DRC Forestry Code adopted by Law No. 11/2002 to encourage sustainable management and socio-economic benefits for local communities 28 .However, there is a lack of specific regulations addressing the unique challenges and opportunities associated with native foods in the country despite the existence of broader policies related to biodiversity management, land use, forestry regulations and agriculture 29 .It is therefore imperative that policies, legislation and regulations to promote the latter be prioritized to encourage their production, marketing and consumption.
Often, research on insect consumption focuses on protein content, whereas high levels of important micronutrients in insects, particularly iron and zinc, can be of significant importance 30 as much as the one reported in nutritious foods such as mushrooms 31 .This is particularly critical, as micronutrient deficiencies are widespread in developing countries, especially among children and breastfeeding women 32 .Edible insects have excellent protein quality 33 , with good amino acid content, energy content, fatty acid profiles and high levels of various micronutrients such as magnesium, manganese, phosphorus, selenium and zinc, as well as the vitamins riboflavin, pantothenic acid, biotin and, in some cases, folic acid 34 .Edible insects also meet the principles of sustainability, accessibility and palatability 35 .
Unlike traditional livestock, standardized information on commercially available edible insects' nutritional composition and sensory quality is limited and inconclusive 36 .However, these limited data are increasingly used to justify generalized claims about the health benefits of a particular genus, order or even insects as a homogeneous food category 23,37 .In several countries, efforts are being made in this direction.However, in the DRC, several species are not yet nutritionally characterized, thus posing a concern about strategies to develop rich foods that would help mitigate food shocks.Given the relevance of edible insects in contributing to food security, it is imperative to assess their true potential.Thus, this study focused not only on assessing the nutritional potential of edible insects in Eastern D.R. Congo, where anthropo-entomophagy practices are widespread, but also on establishing a valuable baseline that could help develop nutritious diets for vulnerable populations still suffering from food insecurity and malnutrition.

Macronutrient composition of commonly consumed edible insects
The macronutrient composition of the edible insects varied significantly (p < 0.05) except for ash content, as depicted in Table 1.While protein content ranged between 20 and 43 g/100 g, fat content ranged between 14 and 36 g/100 g, ash (4 and 6 g/100 g), and moisture content (59 and 77 g/100 g).Concerning protein content, I. oyemensis had the highest protein content, followed by I. epimethea, A. domesticus, R. ferrugineus, R. phoenicis, G.As for texture and aftertaste, N septemfasciata and M. subhyalinus were the most appreciated.After N septemfasciata, Macrotermes subhyalinus, R. differens and L. migratoria were the most appreciated for texture.Gnathocera trivittata, A. mellifera, A. domesticus and R. ferrugineus had the lowest score for texture.Similarly, R. differens, R. phoenicis, N. septemfasciata and L. migratoria were the most appreciated for aftertaste just after M. subhyalinus.Acheta domesticus, G. trivittata, R. ferrugineus and I. oyemensis were the least appreciated for their aftertaste.
A scatter plot of matrices (SPLOM), histograms, and Pearson correlations between sensory attributes and macronutrient composition showed a strong positive correlation between fat content and texture, aftertaste, and overall acceptability, as depicted in Fig. 1.There was a strong correlation between appearance and aftertaste and overall acceptability.Overall acceptability correlated positively with aftertaste, texture, and aroma.Figure 2 showed a SPLOM, histograms, and Pearson correlations between sensory attributes and mineral profile.While a positive correlation was observed between iron and sodium content, a negative correlation was observed between calcium and the latter.In Fig. 3, the principal component analysis (PCA-Biplot) results indicated that the two axes accounted for up to 97.4% of the observed variability in the nutrient composition and sensory attributes of commonly consumed edible insects in the Eastern D. R. Congo.The first and second axes accounted for 86.7% and 10.7% of variability, respectively.

Discussion
The nutritional composition of the edible insects reported in this study varies from one species to another, confirming the variability in nutritional composition of edible insects highlighted in the literature stipulating that the latter may vary according to species, insect life stage, type of insect feeding, habitat 23 , origin 34 , geographical distribution 38 , seasonal 38 and environmental factors 39 and preparation method 40 .In addition, nutritional composition varies between orders 41 and even between species within the same order 34 .Moreover, the macronutrient composition of edible insects in this study is similar to the one reported by Rumpold & Schlüter 34 , who highlighted that the average protein content in edible insects is 40.69 g/100 g and varies between 6.25 and  www.nature.com/scientificreports/71.10 g/100 g, 3.8 and 77.17 g/100 g for fat content, and ash content (1.35 and 12.85 g/100 g) on dry matter.The observed variation in nutritional composition of assessed edible insects are most probably linked to species 42 , feeding 43 , processing methods 40 , geographical sourcing area 38 , and measurement methods.Specifically, the protein, fat, ash, and moisture content of A. domesticus observed in this study is lower than the protein (75.76 g/100 g) and moisture content (70 g/100 g) but higher than the fat (12.93 g/100 g), and ash content (4.54 g/100 g) reported by Bawa et al. 44 .Nevertheless, the macronutrient composition of A. domesticus is similar to the one reported by Montowska et al. 45 , and relatively comparable to that reported by Ayieko et al. 46 , and Oonincx et al. 5 .The macronutrient composition of A. mellifera reported in this study is similar to that reported by Ghosh et al. 47 , except the protein content, which is 35.3 g/100 g for larvae, 45.9 g/100 g (pupae) and 51 g/100 g (adults) on dry matter, and higher than the one reported by Agbidye et al. 48.
Although less documented, the macronutrient composition of G. trivittata species found in this study corroborates that presented by Amouzou et al. 49 in Togo, but with different protein contents.This difference would result from differences in agroecological conditions under which the species was harvested 38,43 .The macronutrient composition of G. africana, I. oyemensis and N. septemfasciata is in some cases superior to that of several conventional meats 23,50,51 , in addition to being tasty 25 , economic 11,18 , and environmentally friendly 52 .
On dry basis matter, the macronutrient composition of I. epimethea is superior to that of the same species purchased alive at local markets in Cameroon 53 , but lower than that degutted I. epimethea presented by Lautenschläger et al. 54 in Angola.The protein content of L. migratoria in this study is lower than that reported in a study from Thailand, but it has a high fat content and similar ash content 55 .In this study, M. subhyalinus presented a macronutrient composition similar to that presented by Kinyuru et al. 41 in Kenya with a protein content of 39.34 g/100 g and ash (7.78 g/100 g) but with a lower fat content (44.82 g/100 g).
Furthermore, the protein and lipid content of R. phoenicis in this study is superior to that reported by Mba et al. 56 in Cameroon and Rumpold and Schlüter 34 , who reported contents varying between 10.3 and 35.6 g/100 g on dry weight basis.The protein (20.4 g/100 g) and ash content (3.5 g/100 g) of R. ferrugineus 57 are lower than those reported in this study.However, they also reported lipid content (38.2 g/100 g) higher than those observed in this study.In this study, the protein content of R. differens was higher than that reported by Ssepuuya et al. 38 .On a dry matter basis; the average protein is similar to that observed in previous studies 58,59 .This study shows that consumption of 100 g of the studied edible insects can contribute to the daily protein requirement of 0.8-1.0g/kg body weight 60 , and therefore, contribute to improving the low daily per capita protein consumption of 55-65 g/ person/day in Sub-Saharan Africa 61 .
As for R. differens, the potassium, sodium, magnesium, iron, calcium and zinc content observed in this study is comparable to the potassium (259.7-370.6 mg/100 g), sodium (229.7-358.7 mg/100 g), magnesium (33.1-33.9mg/100 g), iron (13-16.6 mg/100 g), calcium (24.5-27.4mg/100 g) and zinc (12.4-17.3mg/100 g) content reported by Kinyuru et al. 59 .Low levels of calcium have been reported in R. differens and other grasshoppers as well 64 .Though the low calcium levels can be attributed to insects lacking a mineralized skeleton, animal sources with a mineralized skeleton, such as pork and chicken meat, have a lower calcium content.However, Fombong and collaborators 58 reported higher amounts of calcium, ranging from 977 to 1124 mg/100 g of dried R. differens.This considerable variation within the same species can result from the diet/feed to which the R. differens are exposed in the different sourcing geographical areas and swarming seasons.The sodium content is much lower than that observed in other edible grasshoppers and other edible insects 34 .Though the magnesium content values are similar to those observed by Kinyuru et al. 59 , they are lower than those observed by Fombong et al. 58 in the same species.Compared to pork and chicken meat, R. differens is a better source of dietary macroand micro-mineral elements.Hence, like other animal foods, R. differens can potentially contribute to alleviating the effects of zinc and iron micro-mineral deficiencies, which are among the most important micro-nutrients of public health concern, especially in Africa 65 .
Although poorly documented in terms of mineral profile, the mineral profile of G. africana, I. epimethea, I. oyemensis, L. migratoria, N. septemfasciata and R. ferrugineus observed in this study meets the mineral requirements for adults and children, especially for zinc and iron 66 .It has been observed that locusts have twenty-seven minerals 67 .The mineral content in 100 g of L. migratoria on dry matter varies between 8 and 20 mg 23 .In 2018, a study reported that L. migratoria contains an equal amount of zinc and a higher ratio of iron measured in mg/100 g dry matter and compared to poultry, beef and pork 68 .
In this study, acceptance of edible insects varied from one species to another, confirming the that social and cultural aspects are among the most important elements in their acceptance 69 .The development of delicious and healthy foods containing insects and the adoption of strategies would be an asset for the acceptance of edible insects in countries where their acceptance is still a challenge and are often considered disgusting, although their taste is proven to be mild and easy to accept 10 .Although edible insects are gaining momentum, familiarity seems to be the main driving force, allowing most people to react positively to all edible species in terms of willingness to eat them.Thus, appreciation is linked to availability 70 , ethnicity/culture 71 , palatability 72 , and seasonality 41 .In addition, indigenous knowledge and processing can also influence the appreciation of edible insects 73 .
Findings in this study showed that M. subhyalinus had the highest sensory score, followed by R. differens, N. septemfasciata, R. phoenicis, L. migratoria, G. africana, I. epimethea, A. mellifera, R. ferrugineus, I. oyemensis, G. trivittata and A. domesticus had the lowest sensory score based on overall acceptability, confirming the previous studies of Ishara et al. 24,25 , who found by a survey that R. differens, M. subhyalinus, R. phoenicis and L. migratoria were among the most appreciated edible insects in Eastern Democratic Republic of Congo.Furthermore, previous studies in Portugal 74 , United States of America 75,76 , Italy 77 and Belgium 78 reported that A. domesticus is overall-liked.
Other studies conducted in Nigeria 79 and the USA 75 demonstrated that termites and L. migratoria were overall liked.Moreover, several studies have shown that education would be crucial for a positive attitude towards edible insects among consumers 80 .A study in the Netherlands showed that people who had previously eaten insects had significantly more positive attitudes towards entomophagy than those who had never eaten them and were more likely to eat them again 81 .
The relationship between nutrient composition and sensory acceptance is a dynamic and intricate interplay that significantly influences our food choices, dietary habits, and overall health 82 .It is a complex interplay that involves not only the nutritional value of a food but also how it appeals to our senses, including taste, smell, texture, and appearance 83 .This connection is essential for understanding how the nutritional content of foods impacts their appeal and acceptability among consumers 78 .Taste is a fundamental factor in sensory acceptance.It is closely tied to nutrient composition, although research shows that individuals have variable taste preferences, which can be influenced by genetics and culture 82 .
On the other hand, the aroma of a food, closely linked to its flavour, is another critical aspect of sensory acceptance.Aromas are mainly produced by volatile compounds present in foods, and these compounds are influenced by nutrient composition.Nutrient-rich foods often have more complex and appealing aromas 68 .The texture of a food is essential for sensory acceptance and is determined by nutrient composition 83 .Factors such as fat content, water content and the presence of different textures, such as crunchiness or creaminess, have a significant impact on a food's sensory appeal.Research has shown that fat content influences creaminess and mouthfeel, contributing to sensory satisfaction 84 .Appearance (visual appeal) is an essential component of sensory acceptance.Nutrient composition is vital in food appearance, including color, shape and overall presentation 83 .Attractive colors are often indicative of nutrient richness 85 .A visually appealing food is more likely to be accepted, even before the first bite 85 .

Conclusion and recommendations
The edible insects studied here are highly nutritious, showing their potential as a good source of nutrients with impressive appreciation, underlining their importance in tackling the issues of food insecurity.Although the edible insects studied are nutritionally rich with good sensory scores, these qualities are largely subjected to insect species.In order to fully assess the contribution of the studied edible insects to food and feed security in foodinsecure countries, it is necessary to study their protein quality as a source of essential amino acids and investigate their fatty acids profile, safety, nutrient digestibility and bioavailability as well as the influence of processing on their nutritional quality in addition to encouraging mass rearing to respond to their high existing demand.

Ethics approval
All experimental protocols, as well as methods, were approved and carried out as per relevant guidelines and regulations from the Interdisciplinary Centre for Ethical Research (CIRE) established by the Université Evangélique en Afrique, Bukavu, D.R. Congo, with reference (UEA/SGAC/KM 132/2016).4. The territories were purposely selected for their familiarity with entomophagy practices and unique agroecological conditions, thus influencing edible insects' potential as food and feed.

Sample preparation
Edible insect samples (Fig. 5) from each geographical sourcing area were harvested using traditional methods as described by Ishara et al. 24,25 , then packed in zipping polyethylene bags and delivered to Université Evangelique en Afrique on flaked ice in a cool box before being washed clean and drained.About half of the samples were frozen at − 20 °C shortly until further analyses, and the other half was directly used for sensory assessment purposes.

Macronutrient composition
Macronutrient composition was determined in accordance with the Association of Official Analytical Chemists 86 .While moisture and ash were determined by the hot-air circulating oven (105 °C) and through incineration in a muffle furnace (600 °C) respectively, crude fat content was determined by solvent extraction method using www.nature.com/scientificreports/SoxtecTM2055.Crude protein was determined by the Kjeldahl method and its content was obtained by multiplying the corresponding total nitrogen content by a factor of 5.33 87 .All determinations were carried in triplicate and expressed as mean ± standard error.

Mineral composition
Potassium, Sodium, Magnesium, Iron, Calcium and Zinc were determined in accordance with Association of Official Analytical Chemists 86 .Samples were ashed and the residue dissolved with HCl and filtered using a Whatman filter paper.The mineral content was determined using AA-7000 Atomic Absorption Spectrophotometer (AAS-Shimadzu Corporation, Japan).The absorbance of sample and standard solutions was determined.

Sensory evaluation
Insects were cooked using the methods described by Ishara et al. 24,25 as shown in Table 4. A. domesticus and N. septemfasciata were deep-fried for 7 min, A. mellifera, I. oyemensis, I. epimethea, R. phoenicis and R. ferrugineus were boiled, roasted and deep fried for 10 min, G. trivittata and G. africana were deep-fried for 10 min.Finally, M. subhyalinus and R. differens were fried for 5 min.www.nature.com/scientificreports/Sensory evaluation of the cooked edible insects was carried out at room temperature shortly after cooking by forty panellists from the Université Evangélique en Afrique (UEA).Each cooked edible insect's sample was placed on a small plastic plate and labelled with a random three-digit number.Between sample tests, panellists used neutral non-carbonated mineral water to rinse the mouth.The samples were evaluated in relation to appearance, aroma, taste, texture and overall score was carried out with an intensity-based questionnaire using a 7-point hedonic scale (1 = dislike extremely, 2 = dislike moderately, 3 = dislike slightly, 4 = neither like or dislike, 5 = like slightly, 6 = like moderately and 7 = like extremely) according to Ihekoronye and Ngoddy 88 .

Statistical analysis
Data collected in triplicates were encoded in Microsoft Excel for Mac (Version 16.74).R-Studio Version 4.2.0 and Statistix Version 10 Software were used for statistical analysis including correlation as well as principal component analysis (PCA-Biplot), and data were presented as mean ± standard error.Analysis of variance (ANOVA) was used to compare the nutritional composition and sensory attributes of wild harvested edible insects consumed in the Eastern D.R. Congo.Means were separated using Tukey's test at a significance level of 0.05.

Figure 4 .
Figure 4. Map showing the Democratic Republic of the Congo, the South-Kivu Province, and the study area.

Table 1 .
Macronutrient composition of commonly consumed edible insects.Mean values (n = 3) ± SE.All values except moisture are expressed on dry weight.Values in the same column with the same following letter do not significantly differ (p < 0.05).MC: Moisture content.

Table 2 .
Mineral composition of commonly consumed edible insects in Eastern D. R. Congo (mg/100 g).

Table 3 .
Sensory acceptance of commonly consumed edible insects in Eastern D. R. Congo.Mean values (n = 40) ± SE.Values in the same column with the same following letter do not significantly differ (p < 0.05).
Figure 1.Scatter plot of matrices (SPLOM), histograms, and Pearson correlations between sensory scores and nutrient composition.

Table 4 .
Cooking time and ingredients used.